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@ARTICLE{Brocka:139981,
author = {Brocka, Marta and Helbing, Cornelia and Vincenz, Daniel and
Scherf, Thomas and Montag, Dirk and Goldschmidt, Jürgen and
Angenstein, Frank and Lippert, Michael},
title = {{C}ontributions of dopaminergic and non-dopaminergic
neurons to {VTA}-stimulation induced neurovascular responses
in brain reward circuits.},
journal = {NeuroImage},
volume = {177},
issn = {1053-8119},
address = {Orlando, Fla.},
publisher = {Academic Press},
reportid = {DZNE-2020-06303},
pages = {88-97},
year = {2018},
abstract = {Mapping the activity of the human mesolimbic dopamine
system by BOLD-fMRI is a tempting approach to non-invasively
study the action of the brain reward system during different
experimental conditions. However, the contribution of
dopamine release to the BOLD signal is disputed. To assign
the actual contribution of dopaminergic and non-dopaminergic
VTA neurons to the formation of BOLD responses in target
regions of the mesolimbic system, we used two optogenetic
approaches in rats. We either activated VTA dopaminergic
neurons selectively, or dopaminergic and mainly
glutamatergic projecting neurons together. We further used
electrical stimulation to non-selectively activate neurons
in the VTA. All three stimulation conditions effectively
activated the mesolimbic dopaminergic system and triggered
dopamine releases into the NAcc as measured by in vivo
fast-scan cyclic voltammetry. Furthermore, both optogenetic
stimulation paradigms led to indistinguishable
self-stimulation behavior. In contrast to these
similarities, however, the BOLD response pattern differed
greatly between groups. In general, BOLD responses were
weaker and sparser with increasing stimulation specificity
for dopaminergic neurons. In addition, repetitive
stimulation of the VTA caused a progressive decoupling of
dopamine release and BOLD signal strength, and dopamine
receptor antagonists were unable to block the BOLD signal
elicited by VTA stimulation. To exclude that the sedation
during fMRI is the cause of minimal mesolimbic BOLD in
response to specific dopaminergic stimulation, we repeated
our experiments using CBF SPECT in awake animals. Again, we
found activations only for less-specific stimulation. Based
on these results we conclude that canonical BOLD responses
in the reward system represent mainly the activity of
non-dopaminergic neurons. Thus, the minor effects of
projecting dopaminergic neurons are concealed by
non-dopaminergic activity, a finding which highlights the
importance of a careful interpretation of reward-related
human fMRI data.},
keywords = {Animals / Behavior, Animal: physiology / Brain: diagnostic
imaging / Brain: metabolism / Brain: physiology / Dopamine:
metabolism / Dopamine Antagonists: pharmacology /
Dopaminergic Neurons: physiology / Electric Stimulation /
Electrodes, Implanted / Genetic Vectors / Magnetic Resonance
Imaging: methods / Neurons: metabolism / Neurons: physiology
/ Neurovascular Coupling: physiology / Optogenetics / Rats /
Rats, Long-Evans / Rats, Transgenic / Rats, Wistar / Reward
/ Self Stimulation: physiology / Stereotaxic Techniques /
Tomography, Emission-Computed, Single-Photon / Ventral
Tegmental Area: diagnostic imaging / Ventral Tegmental Area:
metabolism / Ventral Tegmental Area: physiology / Dopamine
Antagonists (NLM Chemicals) / Dopamine (NLM Chemicals)},
cin = {AG Angenstein},
ddc = {610},
cid = {I:(DE-2719)1310004},
pnm = {344 - Clinical and Health Care Research (POF3-344)},
pid = {G:(DE-HGF)POF3-344},
typ = {PUB:(DE-HGF)16},
pubmed = {pmid:29723641},
doi = {10.1016/j.neuroimage.2018.04.059},
url = {https://pub.dzne.de/record/139981},
}